Using a Large-scale Neural Model of Cortical Object Processing to Investigate the Neural Substrate for Managing Multiple Items in Short-term Memory

Many cognitive and computational models have been proposed to help understand working memory. In this article, we present a simulation study of cortical processing of visual objects during several working memory tasks using an extended version of a previously constructed large-scale neural model [Tagamets, M. A., & Horwitz, B. Integrating electrophysiological and anatomical experimental data to create a large-scale model that simulates a delayed match-to-sample human brain imaging study. Cerebral Cortex, 8, 310–320, 1998]. The original model consisted of arrays of Wilson–Cowan type of neuronal populations representing primary and secondary visual cortices, inferotemporal (IT) cortex, and pFC. We added a module representing entorhinal cortex, which functions as a gating module. We successfully implemented multiple working memory tasks using the same model and produced neuronal patterns in visual cortex, IT cortex, and pFC that match experimental findings. These working memory tasks can include distractor stimuli or can require that multiple items be retained in mind during a delay period (Sternberg's task). Besides electrophysiology data and behavioral data, we also generated fMRI BOLD time series from our simulation. Our results support the involvement of IT cortex in working memory maintenance and suggest the cortical architecture underlying the neural mechanisms mediating particular working memory tasks. Furthermore, we noticed that, during simulations of memorizing a list of objects, the first and last items in the sequence were recalled best, which may implicate the neural mechanism behind this important psychological effect (i.e., the primacy and recency effect).

[1]  S. Sternberg Memory-scanning: mental processes revealed by reaction-time experiments. , 1969, American scientist.

[2]  Friedemann Pulvermüller,et al.  A neuroanatomically grounded Hebbian-learning model of attention–language interactions in the human brain , 2008, The European journal of neuroscience.

[3]  J M Fuster,et al.  Neuronal firing in the inferotemporal cortex of the monkey in a visual memory task , 1982, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[4]  Paul M Bays,et al.  Dynamic Shifts of Limited Working Memory Resources in Human Vision , 2008, Science.

[5]  R. Desimone,et al.  Responses of Macaque Perirhinal Neurons during and after Visual Stimulus Association Learning , 1999, The Journal of Neuroscience.

[6]  D. Ts'o,et al.  Visual topography in primate V2: multiple representation across functional stripes , 1995, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[7]  G. E. Alexander,et al.  Neuron Activity Related to Short-Term Memory , 1971, Science.

[8]  Pieter R. Roelfsema,et al.  Remembered but Unused: The Accessory Items in Working Memory that Do Not Guide Attention , 2009, Journal of Cognitive Neuroscience.

[9]  W. Ma,et al.  Changing concepts of working memory , 2014, Nature Neuroscience.

[10]  Y. Miyashita Neuronal correlate of visual associative long-term memory in the primate temporal cortex , 1988, Nature.

[11]  E. Rolls,et al.  Holding Multiple Items in Short Term Memory: A Neural Mechanism , 2013, PloS one.

[12]  Karl J. Friston,et al.  Comparing hemodynamic models with DCM , 2007, NeuroImage.

[13]  T. Sejnowski,et al.  Neurocomputational models of working memory , 2000, Nature Neuroscience.

[14]  A. Baddeley,et al.  The recency effect: Implicit learning with explicit retrieval? , 1993, Memory & cognition.

[15]  R. Desimone,et al.  Neural Mechanisms of Visual Working Memory in Prefrontal Cortex of the Macaque , 1996, The Journal of Neuroscience.

[16]  Adeel Razi,et al.  Dynamic causal modelling revisited , 2017, NeuroImage.

[17]  Carrick C. Williams,et al.  Incidental visual memory for targets and distractors in visual search , 2005, Perception & psychophysics.

[18]  A. Baddeley Working Memory: The Interface between Memory and Cognition , 1992, Journal of Cognitive Neuroscience.

[19]  F. Ashby,et al.  Computational Cognitive Neuroscience , 2017 .

[20]  Leslie G. Ungerleider,et al.  Dissociation of object and spatial visual processing pathways in human extrastriate cortex. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[21]  George A. Alvarez,et al.  Variability in the quality of visual working memory , 2012, Nature Communications.

[22]  John G. Taylor,et al.  A Hard Wired Model of Coupled Frontal Working memories for various Tasks , 1999, Inf. Sci..

[23]  Gustavo Deco,et al.  Large-scale neural model for visual attention: integration of experimental single-cell and fMRI data. , 2002, Cerebral cortex.

[24]  Jieun Kim,et al.  How well does structural equation modeling reveal abnormal brain anatomical connections? An fMRI simulation study , 2009, NeuroImage.

[25]  M. D’Esposito,et al.  Directing the mind's eye: prefrontal, inferior and medial temporal mechanisms for visual working memory , 2005, Current Opinion in Neurobiology.

[26]  Todd S Woodward,et al.  The influence of working memory load on phase specific patterns of cortical activity. , 2004, Brain research. Cognitive brain research.

[27]  D. V. van Essen,et al.  Selectivity for polar, hyperbolic, and Cartesian gratings in macaque visual cortex. , 1993, Science.

[28]  Barry Horwitz,et al.  A Role for Neural Modeling in the Study of Brain Disorders , 2012, Front. Syst. Neurosci..

[29]  D. Hubel,et al.  Orientation columns in macaque monkey visual cortex demonstrated by the 2-deoxyglucose autoradiographic technique , 1977, Nature.

[30]  M. Petrides Dissociable Roles of Mid-Dorsolateral Prefrontal and Anterior Inferotemporal Cortex in Visual Working Memory , 2000, The Journal of Neuroscience.

[31]  P. Goldman-Rakic,et al.  Mnemonic coding of visual space in the monkey's dorsolateral prefrontal cortex. , 1989, Journal of neurophysiology.

[32]  E. Peterhans,et al.  Functional Organization of Area V2 in the Alert Macaque , 1993, The European journal of neuroscience.

[33]  J M Fuster,et al.  Firing changes in cells of the nucleus medialis dorsalis associated with delayed response behavior. , 1973, Brain research.

[34]  H. Kennedy,et al.  A Large-Scale Circuit Mechanism for Hierarchical Dynamical Processing in the Primate Cortex , 2015, Neuron.

[35]  Michel Kerszberg,et al.  A Model for Integrating Elementary Neural Functions into Delayed-Response Behavior , 2006, PLoS Comput. Biol..

[36]  M. R. Riley,et al.  Role of Prefrontal Persistent Activity in Working Memory , 2016, Front. Syst. Neurosci..

[37]  J. Cowan,et al.  Excitatory and inhibitory interactions in localized populations of model neurons. , 1972, Biophysical journal.

[38]  F. T. Husain,et al.  Relating neuronal dynamics for auditory object processing to neuroimaging activity: a computational modeling and an fMRI study , 2004, NeuroImage.

[39]  Raymond J Dolan,et al.  Maintenance versus manipulation in verbal working memory revisited: an fMRI study , 2003, NeuroImage.

[40]  M. D’Esposito,et al.  The neural basis of the central executive system of working memory , 1995, Nature.

[41]  E. Miller,et al.  Suppression of visual responses of neurons in inferior temporal cortex of the awake macaque by addition of a second stimulus , 1993, Brain Research.

[42]  J. Changeux,et al.  A Simple Model of Prefrontal Cortex Function in Delayed-Response Tasks , 1989, Journal of Cognitive Neuroscience.

[43]  P. Goldman-Rakic,et al.  Visuospatial coding in primate prefrontal neurons revealed by oculomotor paradigms. , 1990, Journal of neurophysiology.

[44]  Viktor K. Jirsa,et al.  The Virtual Brain: a simulator of primate brain network dynamics , 2013, Front. Neuroinform..

[45]  O. Sporns,et al.  Mapping the Structural Core of Human Cerebral Cortex , 2008, PLoS biology.

[46]  P S Goldman-Rakic,et al.  Association of Storage and Processing Functions in the Dorsolateral Prefrontal Cortex of the Nonhuman Primate , 1999, The Journal of Neuroscience.

[47]  J. Fuster,et al.  Cellular discharge in the dorsolateral prefrontal cortex of the monkey in cognitive tasks , 1982, Experimental Neurology.

[48]  M. D’Esposito,et al.  The Influence of Working-Memory Demand and Subject Performance on Prefrontal Cortical Activity , 2002, Journal of Cognitive Neuroscience.

[49]  D. Dagenbach,et al.  Patterns of impaired verbal, spatial, and object working memory after thalamic lesions , 2002, Brain and Cognition.

[50]  M. Manosevitz High-Speed Scanning in Human Memory , .

[51]  K. Tanaka,et al.  Divergent Projections from the Anterior Inferotemporal Area TE to the Perirhinal and Entorhinal Cortices in the Macaque Monkey , 1996, The Journal of Neuroscience.

[52]  Brian A. Goolsby,et al.  Distractor devaluation requires visual working memory , 2009, Psychonomic bulletin & review.

[53]  M D'Esposito,et al.  The roles of prefrontal brain regions in components of working memory: effects of memory load and individual differences. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[54]  H. Eichenbaum,et al.  Interplay of Hippocampus and Prefrontal Cortex in Memory , 2013, Current Biology.

[55]  M. Tsodyks,et al.  Working models of working memory , 2014, Current Opinion in Neurobiology.

[56]  R. Desimone,et al.  Visual properties of neurons in area V4 of the macaque: sensitivity to stimulus form. , 1987, Journal of neurophysiology.

[57]  E. Miller,et al.  Timecourse of object‐related neural activity in the primate prefrontal cortex during a short‐term memory task , 2002, The European journal of neuroscience.

[58]  Cheryl L. Grady,et al.  Hemispheric differences in neural systems for face working memory: A PET‐rCBF study , 1995 .

[59]  J. Fuster,et al.  Mnemonic and predictive functions of cortical neurons in a memory task , 1992, Neuroreport.

[60]  Wei Ji Ma,et al.  No Evidence for an Item Limit in Change Detection , 2013, PLoS Comput. Biol..

[61]  M. Hasselmo,et al.  Greater working memory load results in greater medial temporal activity at retrieval. , 2009, Cerebral cortex.

[62]  Leslie G. Ungerleider,et al.  An area specialized for spatial working memory in human frontal cortex. , 1998, Science.

[63]  Kisou Kubota,et al.  Delay-related activity in the primate prefrontal cortex during sequential reaching tasks with delay , 1993, Neuroscience Research.

[64]  Daniel J. Amit,et al.  Paradigmatic Working Memory (Attractor) Cell in IT Cortex , 1997, Neural Computation.

[65]  N. P. Quinn,et al.  Striatal Contribution to Cognition: Working Memory and Executive Function in Parkinson's Disease before and after Unilateral Posteroventral Pallidotomy , 2002, Journal of Cognitive Neuroscience.

[66]  John D. E. Gabrieli,et al.  Reduced working memory span in Parkinson's disease: Evidence for the role of frontostriatal system in working and strategic memory. , 1996 .

[67]  N. Cowan The magical number 4 in short-term memory: A reconsideration of mental storage capacity , 2001, Behavioral and Brain Sciences.

[68]  Antonio Ulloa,et al.  Embedding Task-Based Neural Models into a Connectome-Based Model of the Cerebral Cortex , 2016, Front. Neuroinform..

[70]  Leslie G. Ungerleider,et al.  Contribution of striate inputs to the visuospatial functions of parieto-preoccipital cortex in monkeys , 1982, Behavioural Brain Research.

[71]  Yali Amit,et al.  Modeling behavior in different delay match to sample tasks in one simple network , 2013, Front. Hum. Neurosci..

[72]  S. Sternberg High-Speed Scanning in Human Memory , 1966, Science.

[73]  H. Niki,et al.  Prefrontal cortical unit activity and delayed alternation performance in monkeys. , 1971, Journal of neurophysiology.

[74]  J. A. Horel,et al.  The performance of visual tasks while segments of the inferotemporal cortex are suppressed by cold , 1987, Behavioural Brain Research.

[75]  Reinoud Maex,et al.  The first second: Models of short-term memory traces in the brain , 2009, Neural Networks.

[76]  Boris Suchan,et al.  Involvement of the human medial temporal lobe in a visual discrimination task , 2014, Behavioural Brain Research.

[77]  Antonio Ulloa,et al.  Neural mechanisms of auditory discrimination of long-duration tonal patterns: a neural modeling and fMRI study. , 2008, Journal of integrative neuroscience.

[78]  M. D’Esposito,et al.  Dissecting Contributions of Prefrontal Cortex and Fusiform Face Area to Face Working Memory , 2003, Journal of Cognitive Neuroscience.

[79]  B. Horwitz,et al.  Predicting human functional maps with neural net modeling , 1999, Human brain mapping.

[80]  M. Hasselmo,et al.  Complementary roles of medial temporal lobes and mid‐dorsolateral prefrontal cortex for working memory for novel and familiar trial‐unique visual stimuli , 2013, The European journal of neuroscience.

[81]  Jonathan D. Cohen,et al.  On the Control of Control: The Role of Dopamine in Regulating Prefrontal Function and Working Memory , 2007 .

[82]  John D. E. Gabrieli,et al.  Reduced working memory span in Parkinson's disease: Evidence for the role of frontostriatal system in working and strategic memory. , 1996 .

[83]  B. Horwitz,et al.  Integrating electrophysiological and anatomical experimental data to create a large-scale model that simulates a delayed match-to-sample human brain imaging study. , 1998, Cerebral cortex.

[84]  F. Gregory Ashby,et al.  FROST: A Distributed Neurocomputational Model of Working Memory Maintenance , 2005, Journal of Cognitive Neuroscience.

[85]  Auditory list memory and interference processes in monkeys. , 1999 .

[86]  A. Braun,et al.  Simulating Transcranial Magnetic Stimulation during PET with a Large-Scale Neural Network Model of the Prefrontal Cortex and the Visual System , 2002, NeuroImage.

[87]  G. A. Miller THE PSYCHOLOGICAL REVIEW THE MAGICAL NUMBER SEVEN, PLUS OR MINUS TWO: SOME LIMITS ON OUR CAPACITY FOR PROCESSING INFORMATION 1 , 1956 .

[88]  Michael J. Frank,et al.  Making Working Memory Work: A Computational Model of Learning in the Prefrontal Cortex and Basal Ganglia , 2006, Neural Computation.

[89]  R. Romo,et al.  Neuronal Population Coding of Parametric Working Memory , 2010, The Journal of Neuroscience.

[90]  Howard Eichenbaum,et al.  Distinct Pathways for Rule-Based Retrieval and Spatial Mapping of Memory Representations in Hippocampal Neurons , 2013, The Journal of Neuroscience.

[91]  R. O’Reilly,et al.  A computational approach to prefrontal cortex, cognitive control and schizophrenia: recent developments and current challenges. , 1996, Philosophical transactions of the Royal Society of London. Series B, Biological sciences.